Microtus cabrerae Thomas, 1906

Context and Content. Order Rodentia, suborder Myomorpha, superfamily Muroidea, family Cricetidae, subfamily Arvicolinae, tribe Arvicolini, subgenus Iberomys. The subgenus is monotypic, containing a single extant species and M. cabrerae is currently considered monotypic (see “Nomenclatural Notes”).

Nomenclatural Notes. The species name cabrerae honors Angel Cabrera Latorre (1879–1960), a well-respected mammalogist of the Museu Nacional de Ciencias Naturales in Madrid, who was mentored by Oldfield Thomas from the Natural History Museum in London (Tellado and Molina 2010). Thomas (1906) described the species from a single specimen collected in the same year by Manuel Martínez de la Escalera in Sierra Guadarrama, Spain. In addition to this type specimen, an additional specimen purchased from Émile Parzudaki, who was a natural history dealer, traveller, and collector in Paris, has been in the British Museum since 1853 (Thomas 1906). However, because the collection locality of this specimen was overly general (vaguely described as “Spain”) and may be unreliable, no description was made at that time (Niethammer et al. 1964).

There has been frequent reconsideration of the alignment of M. cabrerae under various subgenera. The species was 1st included in the subgenus Microtus by Pavlinov and Rossolimo in 1987 (Musser and Carleton 2005). Based on archaic morphological characters, Chaline (1972a) used the subgenus Iberomys for M. cabrerae. However, the same author later included the species in the subgenus Arvalomys together with M. arvalis, M. agrestis, and other American voles (Chaline 1974). M. cabrerae was then included in the subgenus Agricola by Zagorodnuyuk in 1990 (Musser and Carleton 2005), although recent phylogenetic data (Jaarola et al. 2004) supported its reclassification under the subgenus Iberomys, as earlier proposed by Chaline (1972a). M. cabrerae is the type and sole extant representative of species from the Iberomys subgenus. Other species included in this subgenus are M. huescarensis (Mazo et al. 1985) and M. brecciensis (Giebel 1847), ancestors of M. cabrerae (e.g., Cabrera-Millet et al. 1983). The subgenus Iberomys has been considered a separate genus from Microtus based on morphology of m1 (Cuenca-Bescós and Laplana 1995; Laplana and Cuenca-Bescós 1998; see “Diagnosis” and “Form”), and I. cabrerae is used by some authors (e.g., López-García 2008). The proposal of elevating the subgenus Iberomys to the genus level has been recently strengthened (Cuenca-Bescós et al., in press), based on morphological distinctiveness from other Microtus (see “Diagnosis”), paleogeographic history (see “Fossil Record”), and certain cytogenetic (see “Genetics) and ecological features (see “Ecology”).

According to Niethammer et al. (1964), M. cabrerae could have been confounded with the species M. asturianus described by Miller (1908), especially because both may occur sympatrically in some localities, such as near Rascafria, where the type specimen of M. cabrerae was collected. However, M. asturianus has long been identified as a subspecies of M. arvalis (e.g., Ellerman and Morrison-Scott 1951). M. dentatus was 1st considered a distinct species (Miller 1910; Cabrera 1914), and later, tentatively recognized as a subspecies of M. cabrerae (Ellerman and Morrison-Scott 1951; Gromov and Polyakov 1992), with M. c. cabrerae occurring mostly in northern and central Iberia, and M. c. dentatus in southeastern Iberia. However, based on morphological (Niethammer et al. 1964; Ayarzagüena and López-Martínez 1976), electrophoretic (Cabrera-Millet et al. 1982), and biometric (Ventura et al. 1998) studies, no valid subspecific variation is currently accepted, and at present M. dentatus is considered a synonym of M. cabrerae. The species was referred to as cabrerai by Trouessart (1910), although the correct spelling of the species name is Thomas' original latinization of Cabrera to cabrerae. An association with M. guentheri was proposed in 1956 by Van den Brink (Niethammer et al. 1964), because this species resembles M. cabrerae in size, and similarly replaces M. arvalis in the southern corner of the Microtus distribution in a disjointed habitat across the southeastern Balkans, Turkey, Syria, Lebanon, Israel, and northern Libya (Musser and Carleton 2005; Grimmberger et al. 2009). However, M. guentheri differs morphologically from M. cabrerae more so than from M. arvalis (Niethammer et al. 1964).

Common names of M. cabrerae vary according to the language and region of origin, including topillo de Cabrera and topillo ibérico (Castilian); talpó de Cabrera (Catalan); Cabrera lursagua (Basque); rato de Cabrera (Portuguese); campagnol de Cabrera, campagnol denté, campagnol méditerranéen, and campagnol Ibérique (French); arvicola di Cabrera (Italian); Cabrera vole, Cabrera's vole, Iberian vole, and Mediterranean vole (English); and Cabreramaus (German). Recently, the Spanish common name Iberón (from Iberomys) has been proposed as an alternative to topillo de Cabrera, mainly for conservation purposes (Cuenca-Bescós et al., in press; see “Conservation”).

DIAGNOSIS

Extant Iberian Microtus species include the semifossorial pine voles Microtus lusitanicus (Lusitanian pine vole, northern Iberia), M. duodecimcostatus (Mediterranean pine vole, southern Iberia), and M. gerbei (Pyrenean pine vole, Pyrenees and eastern Cantabria mountains); the field vole (M. agrestis, northern Iberia); and the common vole (M. arvalis asturianus, northern and central Iberia), which is larger than the nominal subspecies occurring across central and northern Europe (Niethammer et al. 1964; Palomo et al. 2007). Similarly to these species, the length of the tail of M. cabrerae is about one-third the snout–vent length (Niethammer et al. 1964; Madureira and Ramalhinho 1981). However, M. cabrerae (Fig. 1) can be easily distinguished from all these species by its much larger size. The range of physical dimensions of Iberian Microtus provided by Palomo et al. (2007) indicates that body mass of M. cabrerae is about 1.3–4.9 times larger than that of Iberian pine voles, and about 1.0–3.8 larger than that of M. agrestis and M. a. asturianus. The length of the body and tail are, respectively, about 1.1–1.7 and 0.9–2.7 times longer than those of Iberian pine voles, and about 0.8–1.9 and 0.7–1.8 times longer than those of M. agrestis and M. a. asturianus. Ears are relatively long, with length about 1.3–2.5 times longer than that of Iberian pine voles, and about 0.9–1.6 times longer than that of M. a. asturianus and M. agrestis. Also, hind-foot length is larger for M. cabrerae, and provides a particularly useful discriminant feature (usually > 20 mm for M. cabrerae and < 20 mm for all other Iberian Microtus species). As in M. a. asturianus, M. cabrerae has 6 plantar pads, whereas all other Iberian Microtus species have 5.

Fig. 1.

Wild-ranging adult Microtus cabrerae (sex not determined) near Bicos, Odemira, southwestern Portugal (37°48′N, 8°30′W), May 2004. Photograph by Joaquim Pedro Ferreira used with permission.

Microtus cabrerae also displays distinct cranial features (Fig. 2). Its larger size, the smaller incisive capsule on the lower jaw, and the often complex 3rd molar (both M3 and m3), which usually cannot be found in any other Microtus species from the Palearctic (Niethammer et al. 1964; Engels 1972), help distinguish it from other Iberian Microtus species. However, the main characteristic distinguishing M. cabrerae and the Iberomys lineage from other extant rootless-toothed Arvicolinae is the marked transverse asymmetry of the molars, in particular the m1, with wider lingual triangles than labial triangles. In addition, the salient angles are more acute, contrasting with those of other Microtus, Chionomys, and Arvicola species, with rounded salient angles (e.g., Cuenca-Bescós and Laplana 1995; see “Form” for details).

Fig. 2.

Dorsal, ventral, and lateral views of skull and lateral view of the right mandible of an adult female Microtus cabrerae (Museu Bocage—National Museum of Natural History, Lisbon, Portugal, specimen MB01-001208) collected in Grandola, Portugal (38°8′N, 8°33′W) by Inês Rosário on 17 June 2004, donated by Maria da Luz Mathias. Greatest length of skull is 29.8 mm.

Microtus cabrerae is thus easily distinguishable from all other Iberian Microtus species based solely on morphological criteria. However, according to Niethammer et al. (1964), the comparison with M. a. asturianus is particularly relevant because this species may be almost equal in size to M. cabrerae, and both may have been potentially misidentified in the past. Indeed, M. cabrerae resembles M. a. asturianus when it comes to proportions, number of sole pads (6), and number of teats (2 pectoral pairs and 2 inguinal pairs, total = 8). However, the zygomatic arch in M. cabrerae is about 1.3 times wider than in M. a. asturianus, and the nasal bones (nasalia) get less narrow caudally. The incisive foramina are also wider (1.7–2.1 mm compared to 0.9–1.4 mm in M. a. asturianus). Apparently, in contrast to M. a. asturianus, the species has no connected supraorbital cristae, but 2 supraorbital ridges separated by a broad hollow (Niethammer et al. 1964). The mandibular foramen lies further caudally on the top of the ridge of the bone encapsulating the posterior portion of the incisors (as in M. agrestis), which is another characteristic differentiating M. cabrerae from the similar M. a. asturianus (Engels 1972). However, the most probable characteristic distinguishing these species is the much smaller incisive capsule on the lingual side of the processus articularis of the mandible of M. cabrerae. Unlike in M. a. asturianus, the capsule of the lower incisor (i1) in M. cabrerae only continues until the branching point between the processus articularis and the processus angularis. However, like in other Microtus species with a shortened i1, the incisor capsule doesn't completely disappear over the processus articularis, but continues very narrowly (Niethammer et al. 1964). The upper molar rows of M. cabrerae are longer than those of M. a. asturianus (maximum lengths of about 8.0 and 6.8 mm, respectively—Niethammer et al. 1964). Other than the differences in the 3rd molar structure (in particular m3), the species also differ in the pattern of the chewing surface of the M1, which has generally longer and narrower loops in M. cabrerae (Niethammer et al. 1964; see “Form”).

Distinctive features of the fur are the exceptionally long guard hairs in adults, which are more numerous than those of M. agrestis (Niethammer et al. 1964). Guard hairs on the dorsum of M. cabrerae often extend out of the coat about 1 cm, and may have black ends on the distal side, and a subterminal yellow part, giving to the species a more dark yellowish color than in M. agrestis (Niethammer et al. 1964; Engels 1972). Similar but less-prominent guard hair is only known in the Eurasian water vole (Arvicola amphibius—Niethammer et al. 1964). For M. cabrerae, the mean length of the guard hair is almost one-half as high as the down-hair mean length, whereas for M. a. asturianus the guard hair only sticks up one-third of its length out of the down hair (Niethammer et al. 1964). In addition, hair density of adult M. cabrerae is greater than that of M. a. asturianus, and particularly so in relation to M. agrestis (Niethammer et al. 1964). The relatively longer whiskers (vibrissae) also are characteristic of adult M. cabrerae (X̄ ± SE of 26.7 ± 0.48 mm), compared to M. a. asturianus (21.9 ± 0.71 mm) and M. agrestis (22.9 ± 0.60 mm—Niethammer et al. 1964).

GENERAL CHARACTERS

Microtus cabrerae is a medium-sized Arvicolinae species, although among the members of the genus it has one of the largest body masses, with a mean mass of about 52 g, ranging between 30 and 78 g (Ventura et al. 1998; Fig. 1). The general characteristics of the long and thick fur give the coat a rough, brownish olive color on the dorsal side and yellowish tinge on the ventral side (Thomas 1906; Niethammer et al. 1964; Engels 1972). Like other Arvicolinae, juveniles of M. cabrerae are darker in color than subadults and adults. Ears are small and almost completely covered with hair, and the tail is short and slightly bicolored (brownish white above, white below). The long and weighty feet are grayish, and the number of hind-foot sole pads is 6 (Thomas 1906; Engels 1972). No main physical differences are seen between males and females. However, sexual dimorphism in M. cabrerae can be found regarding pelvis dimensions in adult individuals (Ayarzagüena and Cabrera 1976; see “Form”).

Morphometric variability was described in detail by Ventura et al. (1998) from 148 specimens collected between 1977 and 1981 in several localities from different geographic regions across Spain (provinces of Albacete, Cáceres, Cuenca, Madrid, Jaén, Zaragoza, and Huesca), showing no differences in any of the morphological and cranial measurements taken between sexes and among localities. Ventura et al. (1998) provided the following body measurements (mm; mean and range; provinces of Albacete, Cáceres, Cuenca, Madrid, and Jaén): body length, 118.27 (100.00–135.00, n = 51); tail length, 40.48 (30.00–52.00, n = 52); ear length, 13.96 (9.80–16.60, n = 60); hind-foot length, 20.38 (18.20–22.00, n = 63); and the following cranial measurements (mm; mean and range; provinces of Albacete, Cáceres, Cuenca, Madrid, Jaén, Zaragoza, and Huesca): condylobasal length, 28.2 (24.97–30.58, n = 55); condyloincisive length, 28.34 (25.35–30.48, n = 49); nasal length, 9.45 (7.87–10.21, n = 56); incisive foramen length, 5.65 (4.83–8.18, n = 80); upper diastema length, 8.67 (7.21–9.37, n = 77); length of upper molar row (taken from the molar crowns), 6.63 (5.56–7.37, n = 77); braincase height, 8.61 (8.00–9.40, n = 48); braincase height (taken from the tympanic bullae), 11.18 (10.37–11.66, n = 37); interparietal foramen magnum height, 3.64 (3.12–4.54, n = 47); greatest incisive foramen width, 1.85 (1.54–2.22, n = 75); interorbital width, 3.56 (2.98–3.92, n = 69); nasal width, 3.76 (3.04–4.31, n = 76); occipital (or mastoid) width, 12.35 (10.90–13.35, n = 49); zygomatic width, 17.12 (14.66–18.77, n = 55); mandibular length, 18.31 (15.78–19.93, n = 81); length of lower molar row (taken from the molar crowns), 6.55 (5.42–7.38, n = 70); articular height, 9.98 (8.08–10.99, n = 81); and (from Albacete, Cáceres, Madrid, Jaén, Zaragoza, and Huesca): occipitonasal length, 19.02 (17.76–20.37, n = 27); braincase width, 10.51 (9.56–11.41, n = 30); and rostral width, 4.59 (3.88–5.07, n = 74).

DISTRIBUTION

Microtus cabrerae is considered an Iberoccitane endemic, originally occupying the Iberian Peninsula and southern France (e.g., Ayarzagüena and López-Martínez 1976; Cabrera-Millet et al. 1983; Sesé et al. 2011a). The geographical area of the species has globally decreased from the late Pleistocene (about 0.13–0.01 million years ago) to recent times (see “Fossil Record”), and at present, its distribution range is restricted to the Iberian Peninsula (e.g., Ayarzagüena and López-Martínez 1976; Cabrera-Millet et al. 1982; Fernández-Salvador 1998, 2007b; Fernandes et al. 2008; Fig. 3). The 1st episode of range contraction of M. cabrerae took place during the Last Glacial Maximum (late Pleistocene, about 24 thousand years ago), and was followed by an expansion phase during the Holocene Climatic Optimum (Neolithic period, about 8 thousand years ago—Laplana and Sevilla 2013). Climatic warming and aridification during the Bronze Age (Middle Sub-Boreal period, about 5.0–2.5 thousand years ago) are possible reasons to explain the subsequent range contraction of M. cabrerae (Cabrera-Millet et al. 1982; Fernández-Salvador 1998). However, population retraction may have been particularly pronounced from the Iron Age (Sub-Atlantic period, about 2.5 thousand years ago) to present, suggesting that the reduction and fragmentation of the distribution of M. cabrerae may be largely attributed to agricultural expansion since that period (Garrido-García and Soriguer-Escofet 2012; Laplana and Sevilla 2013), which has resulted in the destruction of suitable habitats for the species (see “Conservation”).

Fig. 3.

Current known distribution of Microtus cabrerae in Portugal and Spain (each green dot represents occurrence records of the species mapped at a 10- by 10-km resolution), following Fernández-Salvador (2007b) and Mira et al. (2008), updated with records from local studies (e.g., Rosário and Mathias 2007; Garrido-García et al. 2008, 2013; Ortuño 2009; Pita et al. 2010; and the database from the Conservation Biology Unit, University of Évora). Major rivers (blue lines) and mountain ranges (gray scale) across the Iberian Peninsula also are represented.

Currently, M. cabrerae is reported to occur in the southern and western slopes of the major mountain systems of Iberian Mediterranean areas (e.g., Fernández-Salvador 1998, 2007b; Fernandes et al. 2008; Sesé et al. 2011a; Fig. 3). In Spain it occurs in the Pre-Pyrenees (several localities in Huesca, Zaragoza, and Navarra); Central System (Salamanca, Cáceres, Madrid, and several localities in Ávila and Toledo); Southern Iberian System (Albacete, Cuenca, and a few areas in Murcia and Valencia); Subbetic Sierras (Jaén, and some localities in Málaga and Granada); as well as several areas in Zamora (Vericad 1970, 1971; Ayarzagüena et al. 1975, 1976; Soriguer and Amat 1988; Ayanz 1992; Fernández-Salvador 1998, 2007b; Ventura et al. 1998, and references therein; Garrido-García 1999; Garrido-García et al. 2008; Ortuño 2009). In Portugal the species occurs over the most central region of the country (Estremadura, Ribatejo, Alto Alentejo, and Beira Interior), extending its range to the northeastern side (Trás-os-Montes, Douro Internacional), and to the southwest (western Alentejo and the northwesternmost tip of Algarve—e.g., Queiroz et al. 2005; Mira et al. 2008). Four main, apparently disconnected, areas were recognized: Luso-Carpetano (the largest area), Montibérico, Bético, and Prepirenaico (the smaller and most isolated area—Garrido-García et al. 2013).

The distribution range of M. cabrerae is included in the thermo-, meso-, and supra-Mediterranean bioclimatic zones of Rivas-Martínez (1981), with the species clearly avoiding the Euro-Siberian zone, and regions with particularly high summer temperatures (Mitchell-Jones et al. 1999; Mira et al. 2008). Typically, M. cabrerae occurs in geographical regions characterized by medium rainfall values (between 600 and 1,200 mm), low to medium humidity values (< 85%), and acid to neutral siliceous soils (pH between 3 and 7—Mira et al. 2008) at elevations up to 1,500 m, or limestone substrates up to 800 m (Ayanz 1992; Fernández-Salvador 1998, 2007b).

FOSSIL RECORD

Microtus cabrerae evolved from the radiation of the 1st rootless-toothed voles within the Allophaiomys complex group (Chaline 1970), which were widespread in southern Europe during the early Pleistocene, 2.59–0.78 million years ago (Agusti 1991), and whose presumed ancestor is the Pliocene (5.33–2.59 million years ago) water vole, Mimomys (Ruiz Bustos and Sesé 1985; Chaline and Graf 1988). M. huescarensis (Ruiz Bustos 1988) is the 1st representative of the anagenetic Iberomys lineage, appearing in the Iberian Peninsula by the end of the early Pleistocene, about 0.78 million years ago. The Iberomys lineage is distinguished from other rootless-toothed Arvicolinae by markedly asymmetric, triangle-shaped molars, in particular the m1 (e.g., Cabrera-Millet et al. 1983; Cuenca-Bescós and Laplana 1995; see “Form”). During the middle Pleistocene, about 0.78–0.13 million years ago, M. huescarensis was replaced by M. brecciensis (Giebel 1847), which became the most abundant and widespread vole in the Iberoccitane province (Iberian Peninsula and the Mediterranean region of southern France). M. brecciensis (Hipudaeus brecciensis—Giebel 1847; Forsyth Major 1905) is the direct ancestor of the extant M. cabrerae (Cabrera-Millet et al. 1983), which gradually reduced its distribution range from the late Pleistocene to the present (López-Martínez 2009). Differences in mandible and dental morphologies between M. brecciensis and M. cabrerae were described by Ayarzagüena and López-Martínez (1976) and Sesé et al. (2011b); examination of data suggests that M. cabrerae is larger in size than M. brecciensis.

Archaeological and paleontological sites with fossils of Iberomys (heuscarensis–brecciensis–cabrerae) were thoroughly inventoried by Garrido-García and Soriguer-Escofet (2012) and Laplana and Sevilla (2013). Fossils of M. huescarensis were found at 4 sites in Spain: near Atapuerca (Burgos—Laplana and Cuenca-Bescós 1998; Cuenca-Bescós et al. 1999), Vallparadis, Terrassa (Barcelona—Martínez et al. 2010), Almenara-Casablanca (Castellón—Agustí et al. 2011), and Caravaca de la Cruz (Murcia—Walker et al. 2013).

Fossils of M. brecciensis were found at more than 50 sites from the Iberian Peninsula (including Portugal, Spain, and Britain-Gibraltar), France, and Italy (Garrido-García and Soriguer-Escofet 2012). In addition, fossils described as H. brecciensis were apparently found in the Balkan Peninsula (Marjan, Croatia—Vuletic 1953), although no information on cranial measurements or molar size and structure is available for confirmation. Fossils of M. brecciensis were 1st documented by George Cuvier in 1823 from Sète (Hérault, France—Ayarzagüena and López-Martínez 1976). Fossils of M. brecciensis also were found in other localities in southern France, including Montoussé (Hautes-Pyrénées—Clot 1975), Tautavel (Pyrénées-Orientales—Desclaux 1992), Caniac-du-Causse (Lot—Séronie-Vivien and Tillier 2002), Cénac and Saint Julien (Dordogne—Jeannet and Vital 2009), La Colombière (Hérault—Chaline 1972a), Cèdres Plan d'Aups (Var—Defleur et al. 1990), and Lazaret (Nice, Alpes-Maritimes—Valensi and Abbassi 1998). The most representative records in France are from several localities along the Rhône Valley, such as Soyons (Ardèche—Defleur et al. 2001). The fossils from Saint-Estève-Janson (Bouches-du-Rhône—Chaline 1972a) and Orgnac (Ardèche—Desclaux and Defleur 1997; Jeannet 2000) were particularly important in identifying distinct morphotypes, classified by Chaline (1972a) as M. b. mediterraneus and M. b. orgnasensis, respectively. M. b. mediterraneus was previously described by Chaline (1967) as M. mediterraneus, which was recently synonymized with M. brecciensis (Cuenca-Bescós et al., in press). Late Pleistocene fossils also were found at Plan d'Aups (Var—Defleur et al. 1990), described as M. b. defleuri, and in l'Hortus Cave (Valflaunès, Hérault—Chaline 1972b), described as M. cf. brecciensis mediterraneus-dentatus with characteristics of both M. b. mediterranicus and M. b. organsensis (Chaline 1972b; Ayarzagüena and López-Martínez 1976).

In Spain, middle Pleistocene fossils of M. brecciensis were found at Cúllar de Baza (Granada) by Ruiz Bustos, who 1st assigned the populations to M. b. mediterraneus of St. Esteve Janson (1976) and later (1988) to M. b. brecciensis (Sesé 1989; Ruiz Bustos 1988, 1999; Agustí et al. 2000). Fossils also were found at other localities from Granada, such as Huéscar, Cueva del Agua, and Piñar (Mazo et al. 1985; Sesé 1989; Agustí et al. 2000; López-García 2008), and in several caves in the Atapuerca Mountains (Burgos—e.g., Gil and Sesé 1991; Gil 1997; Cuenca-Bescós et al. 1998, 2001, 2010b; Galindo-Pellicena et al. 2011; López-García et al. 2011c). The relatively wide distribution of M. brecciensis during the middle and late Pleistocene is evidenced by its presence in many localities across Spain, including Torrelaguna, Aranda, and Jarama (Madrid—López-García 2008; Sesé et al. 2011a, 2011b); Buenavista and Salchicha (Toledo—Sesé et al. 2000); Villacastín (Segovia—Arribas 1994); Ambrona (Soria—Sesé 1986); Aguilón (Zaragoza—Cuenca-Bescós et al. 2010a); Gabasa (Huesca—López-García 2008); Bagur (Girona—Martí and Villalta 1974); Baix Penedès and Terrassa (Barcelona—Rabadà 1990; López-García 2007, 2008; Minwer-Barakat et al. 2011); Penedès (Tarragona—Rabadà 1990); Vilafamés (Castellón—Olària et al. 2004–2005); Vilamarxant, Ribera Baixa, and La Valldigna (Valencia—Montañana 1984, 2008, 2010; Peris 2003); Caravaca de la Cruz (Murcia—Walker et al. 2006, 2013); Véles Rubio and Tabernas (Almeria—Delgado-Castilla et al. 1993; Gonzáles-Ramón et al. 2012); El Higuerón (Malaga—López Martínez 1972); ). Valleja (Cádiz—Jennings et al. 2009); and, in Britain, the Devil's Tower (Gibraltar—Garrod et al. 1928).

Middle Pleistocene fossils of M. brecciensis have been found throughout Italy (B. Sala and E. Locateli, in litt.), at localities such as Rifreddo, Sant'Arcangelo Basin (Potenza, Basilicata—Masini et al. 2005); Paglicci Cave near Rignano Garganico (Foggia, Apulia—Colamussi 2002 [not seen, cited in Sala and Locateli 2009]); La Pineta site (Isema, Molise—Sala 1996; Coltorti et al. 2005); Montagnola Senese (Florence, Tuscany—Colamussi 2002 [not seen, cited in Sala and Locateli 2009]); Valdemino Cave near Borgio (Savona, Liguria—Sala and Masini 2007); and Mount Zoppega (Verona, Veneto—Bartolomei 1980 [not seen, cited in Sala and Locateli 2009]). In Portugal, fossils of M. brecciensis were found in Goldra (Loulé, Faro—Antunes et al. 1986), in Caldeirão Cave (Tomar, Santarém—Povoas et al. 1992), and in Aroeira Cave (Torres Novas, Santarém—Marks et al. 2002).

Subfossils of M. cabrerae are relatively common in many late Pleistocene–Holocene deposits in the Iberian Peninsula and southern France. Unlike its ancestor M. brecciensis, M. cabrerae is absent from Italy and the Cantabria region of Spain (Sesé et al. 2011a). In Spain, subfossils of M. cabrerae are known from Maltravieso Cave (Cáceres—Bañuls and López-García 2010; Cardona et al. 2012); Cueva de la Zarzamora (Segovia—Sala et al. 2011); Getafe, Pinilla del Valle, Terralaguna, and Jarama (Madrid—Sesé et al. 2000, 2011a, 2011b; López-García 2008); and Baños de Mula (Murcia—Agusti et al. 1990). Fossils of M. cabrerae also were found in many areas where M. cabrerae is no longer present, including Sant Esteve de la Sarga (Lleida—Oms et al. 2006); Alta Garrotxa and Vilanova de Sau (Girona—López-García 2008); Capellades, Stiges, and Alorda (Barcelona—López-García et al. 2007; López-García and Cuenca-Bescós 2008); Capellades and Vallès Occidental (Barcelona—López-García 2008); Alorda Park (Tarragona—Valenzuela et al. 2009); Albocàsser (Castellon—Sesé 2011); Cabezo Redondo near Villena, Marina Alta, and Moraira-Teulada (Alicante—López-García 2008; Cuñat 2010); Guadix, Baza, and Dorro (Granada—Garrido-García 2008); Alcaucín and Maro (Malaga—López-García 2008); Atapuerca Mountain caves (Burgos—Cuenca-Bescós et al. 2010a; López-García et al. 2010); Becerreá (Lugo—López-García et al. 2011a); and in Britain, Gorham's Cave (Gibraltar—López-García et al. 2011b).

Late Pleistocene and Holocene remains of M. cabrerae found in southern France support the overall contraction of the eastern part of its range up to present (see “Distribution”). Known localities in France with fossil M. cabrerae include Montpellier (Hérault—Heim de Balsac 1939; Ayarzagüena and López-Martínez 1976; Gromov and Polyakov 1992); Montagne Noire (Tarn—Deliry 2009); Bagnères-de-Bigorre (Hautes-Pyrénées—Clot and Evin 1986); Donzère (Drôme—Jeannet and Vital 2009); Bérigoule (Vaucluse—Slimak et al. 2002); and Ardèche (Deliry 2009). In Portugal, remains of M. cabrerae were found in Caldeirão Cave (Tomar, Santarém—Povoas et al. 1992), as well as at Caldas da Rainha (Leiria—Niethammer 1970) and Castro Zambujal (Lisboa—Storch and Uerpmann 1976), from where the species is currently absent.

FORM AND FUNCTION

ONTOGENY AND REPRODUCTION

ECOLOGY

HUSBANDRY

Microtus cabrerae may adapt to laboratory conditions set up to perform short-term studies designed to assess individual-level responses to different experimental treatments (e.g., Mathias et al. 2003; Santos et al. 2004; Rosário et al. 2008; Gomes et al. 2013a, 2013b, 2013c). However, long-standing captive breeding colonies designed to assess reproduction patterns are challenging to maintain (e.g., Fernández-Salvador et al. 2001; Gisbert et al. 2007). In the laboratory, captive M. cabrerae may be housed individually in wire-mesh or glass cages ranging from 40 by 25 by 15 cm up to 70 by 40 by 40 cm (see Mathias et al. 2003; Santos et al. 2004; Rosário et al. 2008; Gomes et al. 2013a), or as breeding pairs in cages of about 120 by 40 by 40 cm (Fernández-Salvador et al. 2001). Captive M. cabrerae may be kept under natural light conditions (Mathias et al. 2003; Santos et al. 2004) or particular photoperiod treatments (e.g., 12L:12D cycles [Fernández-Salvador et al. 2001] or 14L:10D cycles [Gomes et al. 2013a, 2013b, 2013c]), at ambient temperatures ranging between 18°C (Gomes et al. 2013a, 2013b, 2013c) and 26°C (Mathias et al. 2003). Captive M. cabrerae are usually fed a composite diet of apples, carrots, corn, and sunflower seeds, sometimes supplemented with diverse grass species collected at original habitats (Mathias et al. 2003; Santos et al. 2004; Rosário et al. 2008; Gomes et al. 2013a, 2013b, 2013c). Water is provided ad libitum, and cotton and dry grass are often provided as bedding and nesting material (e.g., Fernández-Salvador et al. 2001; Rosário et al. 2008). Cages may be prepared with soil and vegetation from original habitats to allow animals to exhibit their natural behavior, such as burrowing and path building (e.g., Fernández-Salvador et al. 2001; Gomes et al. 2013a, 2013b, 2013c). However, successful captive breeding of M. cabrerae may require that cages are maintained in the field, to more effectively mimic natural conditions (Fernández-Salvador et al. 2001).

GENETICS

Cytogenetic analysis revealed that Microtus cabrerae has a diploid number (2n) of 54 and a fundamental number (FN) of 64 (Díaz de la Guardia et al. 1979; Palacios and Cabrera 1979; Burgos et al. 1988a). Among the contemporary Iberian Microtus species only M. gerbei has the same diploid number (e.g., Musser and Carleton 2005). Other Microtus species occurring in different geographic ranges with a diploid number of 2n = 54 are M. californicus (North America), the Persian vole (M. irani, Iran), and Guenther's vole (M. guentheri, southeastern Balkans, Turkey, Syria, Lebanon, and Israel—Díaz de la Guardia et al. 1979 and references therein). A main feature of the karyotype of M. cabrerae is the presence of enlarged sex chromosomes with large sections of constitutive heterochromatin (known as “giant sex chromosomes”—Díaz de la Guardia et al. 1979; Burgos et al. 1988a; Marchal et al. 2004), a characteristic found in M. agrestis (2n = 50—Burgos et al. 1988a; Jiménez et al. 1991; Marchal et al. 2004; Giménez et al. 2012) and 3 other Microtus species from other geographic areas: the rock vole (M. chrotorrhinus, 2n = 60) from North America, the East European vole (M. levis = epiroticus, 2n = 54) from eastern Europe, and the Transcaspian vole (M. transcaspicus, 2n = 52) from Turkmenistan (Meylan 1967; Marchal et al. 2003, 2004 and references therein). The presence of small to intermediate amounts of heterochromatin in X and Y chromosomes also is known in other Microtus species showing normal- to medium-sized sex chromosomes (e.g., Modi 1987).

The karyotype of M. cabrerae was 1st described by Díaz de la Guardia et al. (1979) as consisting of 3 pairs of large submetacentric chromosomes (pairs 1, 2, and 3), 1 pair of small metacentric chromosomes (pair 4), and 22 pairs (pairs 5–26) of acrocentrics showing gradual differences in size. Variability in chromosome morphology was subsequently shown by Palacios and Cabrera (1979), who classified autosomes of M. cabrerae as follows: 2 pairs of metacentric chromosomes (pairs 1 and 2), 1 pair of submetacentric chromosomes (pair 3), 1 pair of subtelocentrics (pair 4), and 22 pairs of acrocentric–telocentric chromosomes (pairs 5–26), with uniformly distributed sizes. According to Díaz de la Guardia et al. (1979), the 3 biarmed chromosomes pairs 1, 2, and 3 are thought to result from 3 centric fusions (Robertsonian translocation) in an ancestor similar to M. chrotorrhinus, that is, with 2n = 60 and FN = 64. Chromosome banding techniques have additionally shown that autosomes of M. cabrerae have centromeric C-bands larger than those of other Iberian Arvicolinae species (Burgos et al. 1988a; Fernández et al. 2001).

As in M. agrestis and M. chrotorrhinus, the X chromosome in M. cabrerae is a submetacentric giant chromosome (Meylan 1967; Díaz de la Guardia et al. 1979). However, although M. agrestis and M. chrotorrhinus have a giant acrocentric Y chromosome, this chromosome is a giant subtelocentric in M. cabrerae (Marchal et al. 2004). These morphological differences concerning the Y chromosome of M. cabrerae might be the consequence of a pericentric inversion (Díaz de la Guardia et al. 1979), which is the most frequent type of chromosomal rearrangement found in the species (Burgos et al. 1988a). The X chromosome in M. cabrerae constitutes up to 15% of the haploid genome (about 20% in M. agrestis—Marchal et al. 2003, 2004), whereas the relative length of the Y is about 6.5% of the male haploid genome (Díaz de la Guardia et al. 1979). In addition to a euchromatic segment composing the distal three-fourths of the long arm, the X presents a large block of heterochromatin occupying the entire short arm, the centromere, and a one-fourth of the long arm (Burgos et al. 1988a, 1988b; Marchal et al. 2004; Fernández et al. 2001, 2002), whereas in M. agrestis C-band–positive material is distributed over the entire long arm, the centromere, and the proximal part of the short arm (Marchal et al. 2004). In addition, in M. cabrerae a telomeric C-band in the long arm also may be visible in the X chromosomes (Burgos et al. 1988a). As for the Y, similar to M. agrestis, this chromosome has a very long arm composed of constitutive heterochromatin and a very small euchromatic short arm in the pericentromeric region, although respective compositions differ between the species (Burgos et al. 1988c; Fernández et al. 2001, 2002; Marchal et al. 2004).

Similarly to M. agrestis and other Microtus species, the heterochromatin structure in sex chromosomes of M. cabrerae is highly heterogeneous, most likely the result of rapid amplification of blocks of repetitive sequences within the various sections, each with a different origin and composition (Burgos et al. 1988c; Bullejos et al. 1996; Fernández et al. 2001; Marchal et al. 2004). However, there are sequences present in the heterochromatin of the X of M. cabrerae that are absent in the heterochromatin of both sex chromosomes of M. agrestis, as well as in the Y chromosome of M. cabrerae (Fernández et al. 2001, 2002; Marchal et al. 2004). Based on results of G-banding, C-banding, and fluorochrome staining, 6 different subtypes of heterochromatin in the sex chromosomes of M. cabrerae have been described, 4 on the X chromosome and 2 on the Y chromosome (Burgos et al. 1988c; Fernández et al. 2001; Marchal et al. 2004). The X contains large (161-base pair [bp] unit length), late-replicating heterochromatic segments rich in AT base pairs (about 65.84%—Fernández et al. 2001), compared to analogous segments in other rodents (e.g., Bullejos et al. 1996). In M. cabrerae, this tandemly repetitive heterochromatic satellite DNA also is present on 3 interstitial bands in the heterochromatic block of the Y, and in the centromeric region of autosomes (Fernández et al. 2001). In addition, the heterochromatic regions of sex chromosomes of M. cabrerae are frequently involved in chromosomal rearrangements.

A length polymorphism was found in sex chromosomes of M. cabrerae and shown to result from deletion mutations affecting the heterochromatic block of both X and Y (Burgos et al. 1988b), particularly in the repetitive DNA sequences (Fernández et al. 2001). Based on this polymorphism, 3 different X chromosomes (the standard and 2 deleted X chromosomes) and 5 distinct Y chromosomes of different sizes have been described (Burgos et al. 1988b). Some sequences on the X euchromatin of M. cabrerae share homology with the Y euchromatin. Although this region of homology could correspond to pseudoautosomal regions, which are involved in pairing and segregation of chromosomes during meiosis in most mammals, this seems somehow unlikely, because sex chromosomes of M. cabrerae are asynaptic (Marchal et al. 2004).

Another feature of the molecular cytogenetics of M. cabrerae is the presence of multiple copies of the sex-determining region Y (SRY) gene, rather than the single copy observed in most mammal species (Bullejos et al. 1997; Fernández et al. 2002). Although multiple copies of the SRY gene also are found in other Microtus species (Bullejos et al. 1999), in M. cabrerae the SRY gene may be present in both males and females (Fernández et al. 2002), rather than solely in the nonrecombining region of the Y (e.g., Acosta et al. 2010). Fluorescent in situ hybridization determined that copies of SRY (specifically HMG-box copies) occur in the short arm, euchromatic region of the Y, and along the entire heterochromatic region of the X, including the entire short arm, the centromeric region, and the pericentromeric region of the long arm (Fernández et al. 2002). A detailed characterization of the sequence, structure, and organization of the complete SRY copies and their flanking regions, distributed on the X and Y chromosomes, revealed that all sequences are nonfunctional pseudogenes, because they have several premature stop codons resulting from base substitutions and deletions (Marchal et al. 2008). The most likely explanation is that these SRY copies are inactivated by heterochromatinization after their insertion into the constitutive heterochromatin (Fernández et al. 2002). In addition, the presence of different fragments of L1 and LTR retrotransposons in flanking regions may suggest their possible implication in the amplification of the SRY in the Y chromosome, and transportation to the X chromosome heterochromatin (Marchal et al. 2006, 2008). Because the Y chromosome is normally present in males and absent in females, and some cases of sex-reversal XY females have been described in this species (Burgos et al. 1988c), it is possible that 1 functional copy of the SRY gene located on the Y chromosome should act as the testis-determining gene in this species (Fernández et al. 2002). On the other hand, the X chromosome SRY copies must have always been inactive, because the presence of functional copies of this gene in females would give rise to sterile XX males, and consequently X chromosomes containing SRY copies would have been lost from the population (Fernández et al. 2002).

Phylogenetic analysis based on cytochrome-b gene (Cytb) sequences suggests that among the Arvicolinae, the Iberomys lineage seems to be either very old or has undergone accelerated evolution (Jaarola et al. 2004). Support for the basal position of M. cabrerae within the genus Microtus has been recently provided based on amplified fragment length polymorphisms, indicating that similar to M. agrestis, the species does not cluster with the main clade including other European species (Fink et al. 2010). Although its phylogenetic position is still not fully clarified, M. cabrerae can be easily distinguished from other Microtus based on mitochondrial DNA (mtDNA; Cytb and control region) and nuclear sequence (SRY and interphotoreceptor retinoid-binding protein genes) analysis (Alasaad et al. 2010, 2011; Barbosa et al. 2013). The recent development of species-specific primers (e.g., Mika1 and Mika2 for control mtDNA, and SRY-X1, SRY- F, and SRY-inv3 for the SRY gene), as well as the recent advances in DNA extraction protocols based on noninvasive genetic sampling (e.g., feces), have been particularly promising in broadening the repertoire of possible research approaches for studying and monitoring populations of M. cabrerae (e.g., Alasaad et al. 2010, 2011, 2012; Barbosa et al. 2013). However, to date, few studies have used molecular tools to evaluate the levels of genetic diversity and structure in M. cabrerae. Cross-species microsatellite amplification tested in a population from Jaén in Spain has shown high genetic variation (3–10 alleles per locus, varying between 90 and 298 bp) and no deviations from Hardy–Weinberg equilibrium for loci Chni19, Chni09, and Chni18 (European snow vole [Chionomys nivalis]); Moe1, Moe2 (tundra vole [M. oeconomus]); and Mar016, Mar049, Mar079, Mar105, and Mar113 (M. arvalis), thus providing a potential tool for further population genetic studies (Molecular Ecology Resources Primer Development Consortium et al. 2011). In addition, a recent study based on a random amplified polymorphic DNA–polymerase chain reaction technique has shown relatively high genetic diversity and no strong bottleneck events among 3 populations in Spain (Siles, Paterna de Madera, and Valdemorillo de la Sierra) and 1 in Portugal (Bicos), with both the southwest and the east of the Iberia suggested as possible last glacial refugia for the species (Alasaad et al. 2013). Nonetheless, studies including samples collected from more locations, and possibly involving the development of species-specific polymorphic microsatellite markers are still needed to properly reveal the phylogeographic patterns of M. cabrerae, and the extent of population structuring and distinctiveness, as expected from the species' spatial distribution patterns (see “Distribution” and “Population characteristics”).

CONSERVATION

The conservation status of Microtus cabrerae was changed by the International Union for Conservation of Nature and Natural Resources from “Lower Risk/Near Threatened” (Baillie and Groombridge 1996) to “Near Threatened” in 2008, based on its restricted geographic range and reduced estimated area of occupancy (criterion B2), resulting from the severe fragmentation of suitable habitats and related population declines across many areas where the species was present in the past (Fernandes et al. 2008). Indeed, other than the several recent findings of M. cabrerae in some new localities where it was not previously known (e.g., Garrido-García et al. 2008; Ortuño 2009), empirical observations suggest an overall regressive trend of the species at both the regional and local scales (Fernández-Salvador 2007b). For instance, in Spain it is estimated that over the past 10 years, about one-third of populations of M. cabrerae from Cuenca, Toledo, Albacete, and Madrid have disappeared or endured strong modifications. Likewise, populations from Andalucia, Huesca, Zaragoza, Navarra, and Zamora also have undergone strong reductions and high rates of local extinction (Fernández-Salvador 2007b). Population trends in Portugal are not known, but recent steep declines also are suspected across most of its distribution within the country (Queiroz et al. 2005). At the national level the species is thus currently classified as “Vulnerable” in both Spain (criterion B2ab (iii)—Fernández-Salvador 2007b) and Portugal (criterion B2ab (ii, iii, iv, v)—Queiroz et al. 2005), although past national conservation status was “Rare” in both countries (Serviço Nacional de Parques, Reservas e Conservação da Natureza 1990; Blanco and González 1992). M. cabrerae is protected under legislation of the European Union, being included in the Annexes II and IV of the Habitats Directive (Council Directive 92/43/EEC), which imply the designation of special areas of conservation, and the need for strict protection of the species, respectively. The species also is listed as a strictly protected species in Annex II of the Convention on the Conservation of European Wildlife and Natural Habitats (Bern, Switzerland, 1979).

The main threats recurrently associated with populations of M. cabrerae are related to the intensification of human activities reducing the availability of suitable habitats, including agriculture intensification, cattle overgrazing, road construction, and urbanization (e.g., Fernández-Salvador 2007a, 2007b; Pita et al. 2007). In particular, habitat destruction and fragmentation due to farming intensification (land and water management) have been referenced as the most prominent threats for M. cabrerae (e.g., Fernández-Salvador 2007a, 2007b). The nature of habitats of M. cabrerae make them areas highly sought for agriculture conversion, and thus over the past years large amounts of suitable habitat across the species' distribution range have been replaced by intensively managed fields mostly devoted to crop and livestock production (e.g., Landete-Castillejos et al. 2000; Pita et al. 2006, 2007; Fernández-Salvador 2007b). The effects of habitat loss and fragmentation could be particularly pervasive for M. cabrerae because, as a k-strategist (Fernández-Salvador et al. 2001) with low rates of population renewal (Fernández-Salvador et al. 2005b), the species should be particularly vulnerable to the severe environmental change imposed by agricultural intensification (Fernández-Salvador 2007a, 2007b). In addition, the species also may be subjected to strong natural interseasonal and interannual environmental fluctuations (e.g., in local climate conditions) affecting its reproduction success and abundance (e.g., Fernández-Salvador et al. 2001, 2005a; Rosário 2012). For instance, populations from the southwestern limit of the species' distribution range, which is presumably a potentially contracting range margin, have been shown to be particularly responsive not only to habitat fragmentation due to human activities (Pita et al. 2007), but also to the particularly severe and exceptional droughts affecting the region (e.g., in 2005 and 2012), which result in considerable reductions in populations of M. cabrerae, and extremely low recovery abilities (observed by RP). This may indicate that the species may be particularly sensitive to global warming and altering precipitation regimes, which in turn suggests that historic climate changes together with human activities are the main factors causing population declines of M. cabrerae (e.g., Garrido-García and Soriguer-Escofet 2012; Laplana and Sevilla 2013).

Effective conservation of M. cabrerae primarily involves the protection of its habitats at both the local and landscape scale (e.g., Queiroz et al. 2005; Pita et al. 2006, 2007, 2010, 2011b; Fernández-Salvador 2007a; Rosário 2012), eventually requiring some kind of agri-environmental or cross-compliance scheme, whereby farmers could be compensated for maintaining patches of wet grasslands containing the tall vegetation preferred by the species (Pita et al. 2006). Habitat management at the local scale should promote the retention of large habitats (up to 2,000 m²) likely to include several breeding pairs and their maturing offspring (Pita et al. 2010). Efforts should be made to ban waste disposal, and limit operations such as mowing, burning, plowing, or herbicide spraying within habitat patches. Intensive cattle grazing should be avoided, whereas occasional extensive grazing may be considered to prevent eventual habitat degradation due to shrub encroachment (e.g., Fernández-Salvador 1998, 2007a, 2007b; Pita et al. 2006, 2007; Santos et al. 2006). Where local habitats cannot be protected, the translocation of animals from patches that will be affected by human activities (e.g., building of infrastructures such as roads) to other suitable areas could be an option, although its success is still to be evaluated (Gisbert et al. 2007). At the landscape scale attention should be given to the spatial arrangement of habitat patches to prevent isolation of local populations (or clusters of local populations), increasing the chances of both inbreeding and extinction events, while decreasing the likelihood of colonization due to dispersal failure (Pita et al. 2007). Particular importance also should be given to the matrix quality surrounding habitat patches, because it may strongly influence the dispersal abilities of M. cabrerae. In this context, improvement of landscape connectivity toward the long-term persistence of populations of M. cabrerae should consider not only the protection of appropriate habitat-patch networks, but also the maintenance of permeable matrix types, such as seems to be the case of extensively grazed seminatural grasslands (Pita et al. 2007; see “Population characteristics”). Overall, improving the conservation status of M. cabrerae would require the commitment of the central, regional, and local government administrations from both Portugal and Spain, with the need to deepen our understanding on how M. cabrerae responds to environmental changes across multiple spatial and temporal scales.